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The Journal of Neuroscience, December 15, 2000, 20(24):9162-9173
Fine-Tuning an Auditory Synapse for Speed and Fidelity:
Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and
Synaptic Plasticity
Holger
Taschenberger and
Henrique
von Gersdorff
The Vollum Institute, Oregon Health Sciences University, Portland,
Oregon 97201
Fast, precise, and sustained synaptic transmission at high
frequency is thought to be crucial for the task of sound localization in the auditory brainstem. However, recordings from the calyx of Held
synapse have revealed severe frequency-dependent synaptic depression,
which tends to degrade the exact timing of postsynaptic spikes. Here we
investigate the functional changes occurring throughout the critical
period of synapse refinement from immature calyx terminal [postnatal
day 5 (P5)] to after the onset of hearing (P12-P14). Surprisingly,
for recordings near physiological temperature (35°C), we find that
P14 synapses are already able to follow extremely high input rates of
up to 800 Hz. This ability stems in part from a remarkable shortening
of presynaptic action potentials, which may lead to a lowering of
release probability and decrease in synaptic delays during development.
In addition, AMPA receptor-mediated EPSCs as well as quantal synaptic
currents acquired progressively faster kinetics, although their mean
amplitudes did not change significantly. NMDA receptor-mediated EPSCs,
however, diminished with age, as indicated by a 50% reduction in mean
amplitude and faster decay kinetics. Finally, the degree of synaptic
depression was greatly attenuated with age, presumably because of a
2.5-fold or larger increase in the releasable pool of vesicles, which
together with a decreasing release probability produces a fairly
constant EPSC amplitude. This finely tuned orchestra of developmental
changes thus simultaneously promotes speed while preventing premature vesicle pool depletion during prolonged bouts of firing. A few critical
days in postnatal development can thus have a large impact on synaptic function.
Key words:
development; MNTB; calyx of Held; AMPA and NMDA EPSCs; quantal and mEPSCs; short-term synaptic depression; patch-clamp; neuronal reliability
Copyright © 2000 Society for Neuroscience 0270-6474/00/20249162-12$05.00/0
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